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7
Tragedy of the commons
in Melipona bees
Tom Wenseleers* and Francis L. W. Ratnieks
Laboratory of Apiculture and Social Insects, Department of Animal
and Plant Sciences, University of Sheffield, Sheffield S10 2TN, UK
*
Author and address for correspondence: Laboratory of Entomology,
University of Leuven, Naamestraat 59, B-3000 Leuven, Belgium
([email protected]).
Recd 05.11.03; Accptd 22.12.03; Published online 03.03.04
In human society self ish use of common resources
can lead to disaster, a situation known as the ‘tragedy of the commons’ (TOC). Although a TOC is
usually prevented by coercion, theory predicts that
close kinship ties can also favour reduced exploitation. We test this prediction using data on a TOC
occurring in Melipona bee societies.
Keywords: caste conflict; tragedy of the commons;
stingless bees; Melipona
1. INTRODUCTION
Since influential analysis by Hardin (1968) of the ‘tragedy
of the commons’ (TOC), the consensus has been that
coercive management is necessary to prevent overexploitation of common resources such as fish stocks or grazing
land (Hardin 1998; Ostrom 1999). Hardin (1968) argued
that rational individuals benefit from increasing their
share, even if this depletes the resource on which they
depend. In his view, the only way to curb individual selfishness and prevent a TOC was by ‘mutual coercion
mutually agreed upon’ (Hardin 1968). Models developed
by evolutionary theorists (Hamilton 1964; Frank 1995,
1998), however, show an additional mechanism. If the
level of exploitation is heritable and groups are composed
of kin, a rational or ‘evolutionary stable’ exploitation rate
will evolve that is inversely related to genetic relatedness
(Frank 1995, 1998). However, this prediction has never
been tested because in most societies or family groups kinship benefits co-occur with coercion (Mock & Parker
1998), making it impossible to determine their relative
contributions. We test the effects of kinship on the outcome of a TOC that, uniquely, cannot be prevented by
coercion. It concerns the exploitation of a common
resource—the workforce—in Melipona stingless bee
societies.
In highly eusocial bees, such as honeybees and stingless
bees, all work is carried out by morphologically specialized
worker individuals that, like queens, are female (Wilson
1971). The workforce is necessary for colony reproduction, whether by rearing males or by establishing new
colonies via colony fission, in which a queen and a swarm
of workers establish a new nest. Becoming a queen, however, is potentially more rewarding than becoming a
worker since queens have greater reproductive potential
than workers and only queens can ever head daughter colonies (Bourke & Ratnieks 1999; Wenseleers et al. 2003).
So why do more females not attempt to develop as queens
rather than workers? In TOC terms, what prevents the
Proc. R. Soc. Lond. B (Suppl.) 271, S310–S312 (2004)
DOI 10.1098/rsbl.2003.0159
common resource—the workforce—from being exploited
by larvae selfishly choosing to develop into queens? As in
Hardin’s ‘mutual coercion mutually agreed upon’, a TOC
is usually prevented by enforcement (Bourke & Ratnieks
1999). In honeybees (Apis) and most stingless bees
(Trigonini), queens are larger than workers (Wilson
1971). As a result, the adult workers can prevent larval
females from developing into queens by controlling their
access to food (‘nutritional caste determination’; figure 1).
As expected from theory, colonies in these taxa rear few
queens, just enough to permit seasonal swarming or supersedure of a failing mother queen (Wenseleers et al. 2003).
For example, in the honeybee Apis mellifera and in the
trigonine bee Tetragonisca angustula, only ca. 0.02% of all
females develop into queens over a single season (Winston
1987; van Veen & Sommeijer 2000).
Melipona stingless bees are a unique exception to this
pattern (Ratnieks 2001; Wenseleers et al. 2003). In Melipona, the adult workers have little power to control the
caste fate of developing females because queens and workers are the same size, and are reared in identical sealed
cells (Engels & Imperatriz-Fonseca 1990; figure 1). This
gives individual female larvae the power to determine their
own fate (Bourke & Ratnieks 1999; Ratnieks 2001;
Wenseleers et al. 2003; figure 1). Theory shows that in
the pursuit of their individual interests, self-determination
should result in a TOC in which many more immature
females develop into queens than are needed for swarming
(Bourke & Ratnieks 1999; Ratnieks 2001; Wenseleers et
al. 2003). This general prediction is supported because
Melipona colonies greatly overproduce queens (Wilson
1971; Engels & Imperatriz-Fonseca 1990) (5–16% of all
females develop into queens; figure 2). This is costly to
the colony as a whole since the excess queens serve no
useful purpose and are swiftly executed by the workers
after they emerge from their cells (Koedam et al. 1995;
figure 1). However, inclusive fitness theory also makes
more detailed predictions; in particular, that fewer females
should selfishly develop into queens when the cost of
queen overproduction falls on closer kin (Wenseleers et al.
2003). One major factor that affects kinship is the extent
of worker reproduction. Workers can lay male eggs. When
more of the colony’s males are workers’ sons, the cost of
excess queen production is borne by more highly related
individuals, namely workers’ sons (nephews, r = 0.375)
rather than queen’s sons (brothers, r = 0.25). Theory predicts that queen overproduction should be reduced when
more males are workers’ sons (Ratnieks 2001; Wenseleers
et al. 2003). We present the first test, to our knowledge,
of this prediction using data on queen production in
Melipona species with different degrees of worker reproduction (figure 2; see electronic Appendix A).
2. METHODS
(a) Male parentage and caste ratios
To test the effect of kinship on queen production we collated all
available data on male parentage and female caste ratio in Melipona.
A total of 32 studies and four reviews across 13 species were found.
However, we only used studies where male parentage and caste ratio
were known for the same population or geographical region, and were
measured in either their natural environment or laboratory conditions
where conditions approached natural ones as closely as possible. This
produced 12 studies on four species: Melipona beecheii (three studies,
all from Yucatan, Mexico), M. favosa (Tobago, West Indies), M.
quadrifasciata (various sites, Brazil) and M. subnitida (Rio Grande do
Norte, Brazil) (see tables 1, 2 in electronic Appendix A). Male production by workers and female caste ratios in these four species are
S310
 2004 The Royal Society
Tragedy of the commons in bees
(a)
S311
(a)
(d)
Q
(b)
Q
Q
(e)
(c)
Figure 1. In Melipona bees queens are the same size as
workers and develop individually in a sealed cell (bold) on a
provision mass (a). This gives female larvae sufficient
resources to develop into either caste. In other highly
eusocial bees, Trigonini stingless bees (b) and honey bees
(c), the larger queens develop in special cells and their
rearing is under the control of the adult workers who build
and provision the cells. In Melipona, individual control of
caste development results in a TOC in which many more
queens are reared than are needed ((d ) Q, queen pupae in
cells from which cappings have been removed). Excess
queens are killed by workers (left) soon after emergence (e).
summarized in figure 2. Detailed statistics and a complete list of the
original studies are available in electronic Appendix A.
3. RESULTS
As predicted, in species where many males are workers’
sons (M. favosa, Sommeijer et al. 1999; M. quadrifasciata,
da Silva 1977; Tóth et al. 2002; M. subnitida, Contel &
Kerr 1976; Koedam et al. 1999), fewer females selfishly
become queens (5.1–8.6%; Kerr 1950; Koedam et al.
1999; Sommeijer et al. 2003) than in M. beecheii (15.8%;
Darchen & Delage-Darchen 1975; Moo-Valle et al. 2001),
where all males are queens’ sons (Paxton et al. 2001) (see
tables 1 and 2 in electronic Appendix A). In addition,
queen production is lower in M. favosa (5.1%), a species
in which nearly all males are workers’ sons (Sommeijer et
al. 1999), than in M. subnitida (7.1%; Koedam et al. 1999)
and M. quadrifasciata (8.6%; Kerr 1950), where 36–51%
of the males are workers’ sons (see tables 1 and 2 in electronic Appendix A). The negative relationship between
queen overproduction and worker reproduction is significant (␥ = 1, Z = 2.04, p = 0.04) and supports the role of
kinship in influencing a tragedy of the commons. The
observed caste ratios, 5–16%, are slightly lower than those
predicted by theoretical models (14–20%; Wenseleers et
al. 2003). However, these models assume that excess
queen production causes a linear reduction in total colony
productivity (male and swarm production; Wenseleers et
al. 2003). If the cost function were concave, a closer
match between theoretical and empirical figures occurs
4/604/OBS
100
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20
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(b)
percentage of queens
produced
Q
percentage of male
workers’ sons
Q
Proc. R. Soc. Lond. B (Suppl.)
T. Wenseleers and F. L. W. Ratnieks
13/12/10 638
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Figure 2. The effect of the colony kin structure on queen
production in Melipona. Theory predicts that fewer females
should selfishly develop as queens when many males are
workers’ sons because the cost of excess queen production is
then borne by closer relatives, nephews (r = 0.375) rather
than brothers (r = 0.25). This prediction is supported by
levels of queen production in Melipona species with variable
degrees of worker reproduction. In Melipona favosa, where
(a) nearly all males are workers’ sons, and (b) fewer females
selfishly become queens (5.1%) than in M. beecheii (15.8%),
where all males are queen’s sons. In M. subnitida and M.
quadrifasciata, where (a) the queen and the workers share
male parentage, and (b) queen production is intermediate
(7.1 and 8.6%). The negative relationship between queen
overproduction and worker reproduction is significant
(␥ = 1, Z = 2.04, p = 0.04). For each data point the mean,
95% binomial confidence limit and sample size are shown
(number of colonies/months/individuals for queen production
data and number of colonies/males for male parentage data).
For the male parentage data, it is also shown whether the
data come from genetic (GEN) or observational studies
(OBS), or both combined (GEN ⫹ OBS). Significant
( p ⬍ 0.05) and non-significant ( p ⬎ 0.05) differences
between data points, as indicated from a non-overlap of the
confidence limits, are indicated with ‘s’ and ‘n.s.’. A detailed
list of the source studies on which the comparison is based
is given in electronic Appendix A.
(Wenseleers et al. 2003). Importantly, however, a negative
relationship between queen production and worker reproduction is predicted by the theory irrespective of the exact
shape of the cost function. Hence, relative predictions are
robust and independent of detailed assumptions.
4. DISCUSSION
What general lessons can be learned from the way that
bees resolve tragedies of the commons? The Melipona case
shows that in a situation where a common resource is free
to be used by all, selfish exploitation is inevitable (Hardin
1968, 1998). In this respect, Hardin’s conclusion that
S312 T. Wenseleers and F. L. W. Ratnieks
Tragedy of the commons in bees
‘freedom in a commons brings ruin to all’ remains (Hardin
1968, 1998). Not considered by Hardin (1968, 1998),
however, were the effects of kinship. Our results provide
the first tentative evidence, to our knowledge, that kinship
can also partly reduce a TOC. This may be relevant to
human society, such as in cases where common resources
are shared by an extended family. However, coercion is
more effective than kinship in resolving a TOC. Consider
the honeybee A. mellifera. Because of multiple mating by
queens, relatedness among offspring females is low (ca.
0.30), and the optimum proportion of female larvae that
should develop into queens, given the ability to do so, is
very high (56%; Wenseleers et al. 2003). However, excess
queen production in honeybees is effectively prevented
because the adult workers can enforce the caste fate of
larvae by rearing them in distinct cells and on different
foods (Winston 1987; Beekman et al. 2003; figure 1). This
shows that nutritional caste determination, found in most
social Hymenoptera with morphologically distinct queen
and worker castes (Wilson 1971), is actually a form of
social suppression that forces individuals to work for the
benefit of society, even when this is against the individuals’
own selfish interests. In other words, social insect workers
may usually be oppressed rather than genuinely altruistic
(cf. Michener & Brothers 1974; Alonso & Schuck-Paim
2002). In human society, social suppression is also widespread, but fortunately never reaches the point found in
bees where individuals are fated, by their morphology,
to work.
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